Sinking particles promote vertical connectivity in the ocean microbiome

Abstract

The sinking of organic particles formed in the photic layer is a main vector of carbon export into the deep ocean. Although sinking particles are heavily colonized by microbes, so far it has not been explored whether this process plays a role in transferring prokaryotic diversity from surface to deep oceanic layers. Using Illumina sequencing of the 16S rRNA gene, we explore here the vertical connectivity of the ocean microbiome by characterizing marine prokaryotic communities associated with five different size fractions and examining their compositional variability from surface down to 4,000 m across eight stations sampled in the Atlantic, Pacific, and Indian Oceans during the Malaspina 2010 Expedition. Our results show that the most abundant prokaryotes in the deep ocean are also present in surface waters. This vertical community connectivity seems to occur predominantly through the largest particles because communities in the largest size fractions showed the highest taxonomic similarity throughout the water column, whereas free-living communities were more isolated vertically. Our results further suggest that particle colonization processes occurring in surface waters determine to some extent the composition and biogeography of bathypelagic communities. Overall, we postulate that sinking particles function as vectors that inoculate viable particle-attached surface microbes into the deep-sea realm, determining to a considerable extent the structure, functioning, and biogeography of deep ocean communities.

Keywords: connectivity; deep ocean; dispersion; marine prokaryotic metacommunities; particle sinking.

Fig. 1.

nMDS ordinations representing spatially the Bray–Curtis distances between the prokaryotic communities studied. Distances were calculated using the rarefied OTU table. Samples are color-coded depending on (A) size fraction, (B) depth, and (C) sampling station.

Fig. 2.

Contribution of the OTUs categorized as surface (SFC), deep-chlorophyll maximum (DCM), mesopelagic (MESO), and bathypelagic (BATHY), in each depth and size fraction, expressed as (A) percentage of OTUs and (B) percentage of sequences. The category of each OTU was defined as the depth where they were first detected, considering a directionality from surface to bathypelagic waters, and considering all stations together (see Materials and Methods for details).

Fig. 3.

Vertical variation in (A) beta diversity (i.e., community differentiation), (B) spatial OTU turnover (i.e., species replacement), (C) nestedness (species loss), and (D) niche breadth (i.e., habitat specialization of the OTUs based on the number of depths where an OTU was detected) for each size fraction. Values were calculated among depths, for each size fraction, and separately for each station. Boxplots summarize the data from the eight stations. Beta diversity comprised values from 1 to 4, where 1 indicates that all OTUs from the four depths are the same and 4 indicates that OTUs from the four depths are completely different. Beta diversity can be partitioned into two components: turnover and nestedness. Turnover indicates the replacement of some OTUs by others from depth to depth, and nestedness indicates the subset of OTUs from one depth to the other. Both turnover and nestedness comprised values from 0 to 1, indicating the level of contribution to beta diversity. Niche breadth was calculated for each OTU, indicating the number of depths where an OTU was found. Values ranged from 1 to 4, where 4 indicates that a given OTU is present at the four depths (i.e., higher values of the boxplot indicate that the OTUs of a given size fraction were present across more depths). See Materials and Methods for more details.

Fig. 4.

Vertical variation of the contribution (in percentage of sequences) of surface OTUs enriched in small size fractions (PAN-Index < 2.7) (light gray) and surface OTUs enriched in large size fractions (PAN-Index ≥ 2.7) (dark gray) to communities present in (A) fractions <3.0 µm and (B) fractions ≥3.0 µm and at each depth. The boxplots summarize the data from the eight stations. See Materials and Methods for further details.

Fig. 5.

Dynamics of seed OTUs at each station and across depths. Seed OTUs are the surface OTUs enriched in the larger size fractions that increase in relative abundance with depth. Data represent the contribution of the OTUs categorized as seeds to the total sequences of communities associated to the largest size fractions (≥3.0 µm; see Results for details). Pie charts indicate the taxonomic composition at the order level (in percentage of sequences) of the seed OTUs at each station. Note the different scales in the graphs.